Memory Modulates Journey-Dependent Coding in the Rat Hippocampus

Abstract

Neurons in the rat hippocampus signal current location by firing in restricted areas called place fields. During goal-directed tasks in mazes, place fields can also encode past and future positions through journey-dependent activity, which could guide hippocampus-dependent behavior and underlie other temporally extended memories, such as autobiographical recollections. The relevance of journey-dependent activity for hippocampal-dependent memory, however, is not well understood. To further investigate the relationship between hippocampal journey-dependent activity and memory we compared neural firing in rats performing two mnemonically distinct but behaviorally identical tasks in the plus maze: a hippocampus-dependent spatial navigation task, and a hippocampus-independent cue response task. While place, prospective, and retrospective coding reflected temporally extended behavioral episodes in both tasks, memory strategy altered coding differently before and after the choice point. Before the choice point, when discriminative selection of memory strategy was critical, a switch between the tasks elicited a change in a field’s coding category, so that a field that signaled current location in one task coded pending journeys in the other task. After the choice point, however, when memory strategy became irrelevant, the fields preserved coding categories across tasks, so that the same field consistently signaled either current location or the recent journeys. Additionally, on the start arm firing rates were affected at comparable levels by task and journey, while on the goal arm firing rates predominantly encoded journey. The data demonstrate a direct link between journey-dependent coding and memory, and suggest that episodes are encoded by both population and firing rate coding.

Dynamic coding of dorsal hippocampal neurons between tasks that differ in structure and memory demand

“…Consistent with previous studies (Markus et al, 1995; Ferbinteanu et al, 2011), our results demonstrate that hippocampal place fields can remap to flexibly represent changes in task (task remapping), as a subpopulation of hippocampal neurons with place fields on the T-maze showed high spatial correlation between alternation epochs (same task), and low spatial correlation between either alternation epoch and the CD epoch (different tasks). This result indicates that place cells are sensitive to changes in behavioral strategy even in the absence of changes to the recording environment and behavioral apparatus.…”

“…Recent studies have supported these findings by demonstrating that trajectory coding on the stem of a T-maze that signals the journey of the rat during an alternation task does not respond to the introduction of a visual or tactile cue on the maze stem that signals reward location, indicating that memory retrieval and trajectory coding can occur independently of one another (Ainge et al, 2012; Griffin et al, 2012). Furthermore, when rats switch between a hippocampal-dependent spatial navigation task and a non hippocampal-dependent cue-approach task in a plus maze, both prospective and retrospective trajectory coding is seen in equal proportion during both tasks, arguing against the interpretation that trajectory coding is a reflection of hippocampal-dependent episodic memories (Ferbinteanu et al, 2011). …”

Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex

“…An interesting counterpoint to these data comes from work that examined OFC and hippocampal coding throughout the course of entire trials 91–95 . These experiments tested rats on a plus-shaped maze.…”

“…Hippocampal neurons recorded on the task showed spatial responses that were strongly context- or state-dependent 91,94,96 . For instance, a place field located on the south start arm might only be active as the animal ran towards the west goal arm, showing no firing at all when the animal passed in the same direction through the identical location en route to the east goal arm.…”

“…Whereas neurons in the hippocampus encoded context information about rats’ journeys while preserving single-cell representations of position, neurons in the OFC seemed to average across large swaths of space, placing a premium on outcome encoding 91,97 . This suggests that cognitive maps in the hippocampus and OFC might contain similar types of information but that they might format this information in different ways.…”